Recombination Alters the Dynamics of Adaptation on Standing Variation in Laboratory Yeast Populations

The rates and selective effects of beneficial mutations, together with population genetic factors such as population size and recombination rate, determine the outcomes of adaptation and the signatures this process leaves in patterns of genetic diversity. Previous experimental studies of microbial evolution have focused primarily on initially clonal populations, finding that adaptation is characterized by new strongly selected beneficial mutations that sweep rapidly to fixation. Here, we study evolution in diverse outcrossed yeast populations, tracking the rate and genetic basis of adaptation over time. We combine time-serial measurements of fitness and allele frequency changes in 18 populations of budding yeast evolved at different outcrossing rates to infer the drivers of adaptation on standing genetic variation. In contrast to initially clonal populations, we find that adaptation is driven by a large number of weakly selected, linked variants. Populations undergoing different rates of outcrossing make use of this selected variation differently: whereas asexual populations evolve via rapid, inefficient, and highly variable fixation of clones, sexual populations adapt continuously by gradually breaking down linkage disequilibrium between selected variants. Our results demonstrate how recombination can sustain adaptation over long timescales by inducing a transition from selection on genotypes to selection on individual alleles, and show how pervasive linked selection can affect evolutionary dynamics.

[1]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[2]  H. Muller Some Genetic Aspects of Sex , 1932, The American Naturalist.

[3]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .

[4]  R. Lewontin The Interaction of Selection and Linkage. I. General Considerations; Heterotic Models. , 1964, Genetics.

[5]  M. Kimura Attainment of Quasi Linkage Equilibrium When Gene Frequencies Are Changing by Natural Selection. , 1965, Genetics.

[6]  M. Kimura,et al.  Evolution in Sexual and Asexual Populations , 1965, The American Naturalist.

[7]  W. G. Hill,et al.  The effect of linkage on limits to artificial selection. , 1966, Genetical research.

[8]  M. Feldman,et al.  On the evolutionary effect of recombination. , 1970, Theoretical population biology.

[9]  J. M. Smith,et al.  The hitch-hiking effect of a favourable gene. , 1974, Genetical research.

[10]  S. Karlin General two-locus selection models: some objectives, results and interpretations. , 1975, Theoretical population biology.

[11]  M. Bulmer The Mathematical Theory of Quantitative Genetics , 1981 .

[12]  J. Wagstaff,et al.  Mechanisms of Mitotic Recombination , 1981 .

[13]  R. Elston The mathematical theory of quantitative genetics , 1982 .

[14]  T. Petes,et al.  Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes. , 1986, Genetics.

[15]  H. Klein Recombination between repeated yeast genes , 1988 .

[16]  J. Haber,et al.  Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. , 1989, Genetics.

[17]  J. Gillespie The causes of molecular evolution , 1991 .

[18]  S. Jinks-Robertson,et al.  Allelic and ectopic interactions in recombination-defective yeast strains. , 1991, Genetics.

[19]  J. Peck A ruby in the rubbish: beneficial mutations, deleterious mutations and the evolution of sex. , 1994, Genetics.

[20]  J. Phillips,et al.  The Role of DNA Double-Strand-Break Rejoining in Chromosome Damage and Repair , 1994 .

[21]  R. Green,et al.  IS A LITTLE BIT OF SEX AS GOOD AS A LOT , 1995 .

[22]  N. Barton Linkage and the limits to natural selection. , 1995, Genetics.

[23]  G. Bell,et al.  The advantage of sex in evolving yeast populations , 1997, Nature.

[24]  M. Conrad,et al.  Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. , 1997, Science.

[25]  J. Gillespie Genetic drift in an infinite population. The pseudohitchhiking model. , 2000, Genetics.

[26]  J. Gillespie IS THE POPULATION SIZE OF A SPECIES RELEVANT TO ITS EVOLUTION? , 2001, Evolution; international journal of organic evolution.

[27]  T. Johnson,et al.  The effect of deleterious alleles on adaptation in asexual populations. , 2002, Genetics.

[28]  Pardis C Sabeti,et al.  Detecting recent positive selection in the human genome from haplotype structure , 2002, Nature.

[29]  N. Colegrave Sex releases the speed limit on evolution , 2002, Nature.

[30]  L. Rieseberg,et al.  Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization , 2003, Science.

[31]  T. Rocheford,et al.  Maize selection passes the century mark: a unique resource for 21st century genomics. , 2004, Trends in plant science.

[32]  R. Nielsen,et al.  Linkage Disequilibrium as a Signature of Selective Sweeps , 2004, Genetics.

[33]  David Botstein,et al.  GO: : TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes , 2004, Bioinform..

[34]  W. Ewens Mathematical Population Genetics : I. Theoretical Introduction , 2004 .

[35]  J. Hermisson,et al.  Soft Sweeps , 2005, Genetics.

[36]  J. Coffin,et al.  Evolution of Human Immunodeficiency Virus Under Selection and Weak Recombination , 2005, Genetics.

[37]  Christopher R. Jones,et al.  Sex increases the efficacy of natural selection in experimental yeast populations , 2005, Nature.

[38]  Hye-Jung E. Chun,et al.  Genomic Convergence toward Diploidy in Saccharomyces cerevisiae , 2006, PLoS genetics.

[39]  L. Andersson,et al.  Epistasis and the release of genetic variation during long-term selection , 2006, Nature Genetics.

[40]  Robert J. D. Reid,et al.  The Role of DNA Double-Strand Breaks in Spontaneous Homologous Recombination in S. cerevisiae , 2006, PLoS genetics.

[41]  J. Pritchard,et al.  A Map of Recent Positive Selection in the Human Genome , 2006, PLoS biology.

[42]  John Maynard Smith,et al.  The hitch-hiking effect of a favourable gene. , 1974, Genetical research.

[43]  A. Clark,et al.  Recent and ongoing selection in the human genome , 2007, Nature Reviews Genetics.

[44]  T. Cooper Recombination Speeds Adaptation by Reducing Competition between Beneficial Mutations in Populations of Escherichia coli , 2007, PLoS biology.

[45]  L. Steinmetz,et al.  High-resolution mapping of meiotic crossovers and non-crossovers in yeast , 2008, Nature.

[46]  David B. Witonsky,et al.  Adaptations to Climate in Candidate Genes for Common Metabolic Disorders , 2008, PLoS genetics.

[47]  F. Hospital,et al.  Selective Sweep at a Quantitative Trait Locus in the Presence of Background Genetic Variation , 2008, Genetics.

[48]  D. Schluter,et al.  Adaptation from standing genetic variation. , 2008, Trends in ecology & evolution.

[49]  D. Botstein,et al.  The cost of gene expression underlies a fitness trade-off in yeast , 2009, Proceedings of the National Academy of Sciences.

[50]  Robert P. Davey,et al.  Population genomics of domestic and wild yeasts , 2008, Nature.

[51]  Jeffrey E. Barrick,et al.  Genome evolution and adaptation in a long-term experiment with Escherichia coli , 2009, Nature.

[52]  A. Weismann Essays Upon Heredity and Kindred Biological Problems , 2009 .

[53]  Arvind Gupta,et al.  Data reduction for spectral clustering to analyze high throughput flow cytometry data , 2010, BMC Bioinformatics.

[54]  P. Phillips,et al.  Mutation load and rapid adaptation favour outcrossing over self-fertilization , 2009, Nature.

[55]  B. Shraiman,et al.  Competition between recombination and epistasis can cause a transition from allele to genotype selection , 2009, Proceedings of the National Academy of Sciences.

[56]  Kevin R. Thornton,et al.  Genome-wide analysis of a long-term evolution experiment with Drosophila , 2010, Nature.

[57]  David B. Witonsky,et al.  Adaptations to new environments in humans: the role of subtle allele frequency shifts , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[58]  Mats E. Pettersson,et al.  Genome-Wide Effects of Long-Term Divergent Selection , 2010, PLoS genetics.

[59]  Eric C. Rouchka,et al.  Proceedings of the ninth annual UT-ORNL-KBRIN Bioinformatics Summit 2010 , 2008, BMC Bioinformatics.

[60]  F. Ayala,et al.  Human Adaptations to Diet, Subsistence, and Ecoregion Are Due to Subtle Shifts in Allele Frequency , 2010 .

[61]  B. Shraiman,et al.  Rate of Adaptation in Large Sexual Populations , 2010, Genetics.

[62]  M. Goddard,et al.  Sex enhances adaptation by unlinking beneficial from detrimental mutations in experimental yeast populations , 2012, BMC Evolutionary Biology.

[63]  S. van Noort,et al.  Codivergence and multiple host species use by fig wasp populations of the Ficus pollination mutualism , 2012, BMC Evolutionary Biology.

[64]  Alan M. Moses,et al.  Revealing the genetic structure of a trait by sequencing a population under selection. , 2011, Genome research.

[65]  B. Shraiman,et al.  Statistical genetics and evolution of quantitative traits , 2011, 1108.1630.

[66]  Michael M. Desai,et al.  Genetic Variation and the Fate of Beneficial Mutations in Asexual Populations , 2011, Genetics.

[67]  Nigel F. Delaney,et al.  Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation , 2011, Science.

[68]  M. Mézard,et al.  Emergence of clones in sexual populations , 2012, 1205.2059.

[69]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[70]  M. Burke How does adaptation sweep through the genome? Insights from long-term selection experiments , 2012, Proceedings of the Royal Society B: Biological Sciences.

[71]  R. Gibbs,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:Epistasis dominates the genetic architecture of Drosophila quantitative traits , 2012 .

[72]  H. Hoekstra,et al.  EVIDENCE OF ADAPTATION FROM ANCESTRAL VARIATION IN YOUNG POPULATIONS OF BEACH MICE , 2012, Evolution; international journal of organic evolution.

[73]  Cameron D. Palmer,et al.  Evidence of widespread selection on standing variation in Europe at height-associated SNPs , 2012, Nature Genetics.

[74]  C. Schlötterer,et al.  Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles , 2012, Molecular ecology.

[75]  Y. Pilpel,et al.  Chromosomal duplication is a transient evolutionary solution to stress , 2012, Proceedings of the National Academy of Sciences.

[76]  Michael J. Wiser,et al.  Long-Term Dynamics of Adaptation in Asexual Populations , 2013, Science.

[77]  Michael M. Desai,et al.  Pervasive Genetic Hitchhiking and Clonal Interference in 40 Evolving Yeast Populations , 2013, Nature.

[78]  Daniel J. Kvitek,et al.  Whole Genome, Whole Population Sequencing Reveals That Loss of Signaling Networks Is the Major Adaptive Strategy in a Constant Environment , 2013, PLoS genetics.

[79]  B. Shraiman,et al.  Coalescence and genetic diversity in sexual populations under selection , 2013, Proceedings of the National Academy of Sciences.

[80]  Philipp W. Messer,et al.  SLiM: Simulating Evolution with Selection and Linkage , 2013, Genetics.

[81]  R. Neher Genetic Draft, Selective Interference, and Population Genetics of Rapid Adaptation , 2013, 1302.1148.

[82]  Daniel B. Weissman,et al.  The Rate of Adaptation in Large Sexual Populations with Linear Chromosomes , 2013, Genetics.

[83]  Michael M. Desai,et al.  Global epistasis makes adaptation predictable despite sequence-level stochasticity , 2014, Science.

[84]  Benjamin H. Good,et al.  Genetic Diversity in the Interference Selection Limit , 2014, PLoS genetics.

[85]  Nishtha Agrawal Competition Between Recombination and Chromosome Organization in Salmonella Typhimurium , 2014 .

[86]  Jeffrey E. Barrick,et al.  Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. , 2014, Methods in molecular biology.

[87]  Benjamin H. Good,et al.  The Impact of Macroscopic Epistasis on Long-Term Evolutionary Dynamics , 2014, Genetics.

[88]  G. Coop,et al.  A Population Genetic Signal of Polygenic Adaptation , 2013, PLoS genetics.

[89]  A. Long,et al.  Standing genetic variation drives repeatable experimental evolution in outcrossing populations of Saccharomyces cerevisiae. , 2014, Molecular biology and evolution.

[90]  Phillip A. Richmond,et al.  Polyploidy can drive rapid adaptation in yeast , 2015, Nature.

[91]  Benjamin H. Good,et al.  Fate of a mutation in a fluctuating environment , 2015, Proceedings of the National Academy of Sciences.

[92]  A. Long,et al.  Elucidating the molecular architecture of adaptation via evolve and resequence experiments , 2015, Nature Reviews Genetics.

[93]  P. Bayrak-Toydemir,et al.  Hereditary hemorrhagic telangiectasia: genetics and molecular diagnostics in a new era , 2015, Front. Genet..

[94]  O. Tenaillon,et al.  The rule of declining adaptability in microbial evolution experiments , 2015, Front. Genet..

[95]  J. Bouchaud,et al.  Why Do Markets Crash? Bitcoin Data Offers Unprecedented Insights , 2015, PloS one.

[96]  J. Berman,et al.  Shift and adapt: the costs and benefits of karyotype variations , 2015, bioRxiv.

[97]  Maitreya J. Dunham,et al.  The Fitness Consequences of Aneuploidy Are Driven by Condition-Dependent Gene Effects , 2015, PLoS biology.

[98]  Tami D. Lieberman,et al.  Inexpensive Multiplexed Library Preparation for Megabase-Sized Genomes , 2015, bioRxiv.

[99]  Sasha F. Levy,et al.  Development of a Comprehensive Genotype-to-Fitness Map of Adaptation-Driving Mutations in Yeast , 2016, Cell.

[100]  Michael M. Desai,et al.  Sex Speeds Adaptation by Altering the Dynamics of Molecular Evolution , 2016, Nature.

[101]  Franziska Wulf,et al.  Mathematical Population Genetics , 2016 .

[102]  S. Ranque,et al.  Environmental distribution of Cryptococcus neoformans and C. gattii around the Mediterranean basin. , 2016, FEMS yeast research.

[103]  J. Berman Ploidy plasticity: a rapid and reversible strategy for adaptation to stress. , 2016, FEMS yeast research.

[104]  Kyle J. Gaulton,et al.  Detection of human adaptation during the past 2000 years , 2016, Science.

[105]  P. David,et al.  Experimental Evidence for the Negative Effects of Self-Fertilization on the Adaptive Potential of Populations , 2017, Current Biology.

[106]  N. Saitou,et al.  Population Genomics , 2019, Population Genomics.